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Abstract Lactic acid bacteria have been important industrial floras in the food fermentation production industry since ancient times. Their metabonomics technology has been widely used in the process monitoring, product classification and flavor formation mechanism of lactic acid bacteria-fermented foods. In this study, we discussed the application status of metabonomics technology in lactic acid bacteria-fermented food industry and scientific research, including dairy products, soy products, beverages and some pickled foods. Metabolomics will be applied in the research fields of lactic acid bacteria metabolism mechanism of lactic acid bacteria-fermented foods, lactic acid bacteria metabolomics database construction and expansion, metabolomics and genomics, and proteomics. In particular, the metabolomics technology will be introduced into product development and quality monitoring of traditional Chinese lactic acid bacteria-fermented foods, such as fermented bean curd and suancai, thereby perfecting industry norms and improving the level of industry development.
Key words Metabolomics; Lactic acid bacteria; Fermentation; Food
Received: February 14, 2021 Accepted: April 17, 2021
Supported by Yantai Science and Technology Planing Project (2019ZDCX013); High-efficiency Ecological Agriculture Innovation Project of Taishan Industry Leading Talent Engineering (LJNY202001); Key R&D Program of Shandong Province (2019GNC106019).
Guangpeng LIU (1984-), male, P. R. China, researcher, devoted to research about fruit and vegetable fermentation.
*Corresponding author. E-mail: [email protected].
Lactic acid bacteria have been involved in many fermented food production processes as common strains in fermented foods since ancient times, such as dairy products［1］, soy products［2］, drinks［3-4］ and some pickled foods［5］. The metabolic activities of lactic acid bacteria are closely related to the flavor, aroma, texture and nutrition of fermented foods. With the development of metabonomics technology, this technology has been widely used in the research of monitoring the process of lactic acid bacteria-fermented foods and the formation mechanism of characteristic flavor substances.
Lactic acid bacteria will produce a large number of metabolites during fermentation, including organic acids, amino acids, oligosaccharides, small peptides and some aromatic substances, etc., and revealing the relationship between these metabolites and their influencing factors is of great significance for improving the quality of fermented foods based on lactic acid bacteria and optimizing the fermentation process. The comprehensiveness and high resolution of metabolomics can comprehensively evaluate and discover the subtle differences between samples, so it can provide conclusive and quantitative data for lactic acid bacteria-fermented foods, fermentation process optimization and product quality improvement. Application of Metabonomics in Lactic Acid Bacteria-fermented Drinks
In addition to being widely used in fermented milk and fermented vegetables, lactic acid bacteria also play an important role in the fermentation of some fermented beverages and wines. Lee et al.［20］ used Oenococcus oeni in malolactic fermentation (MLF) of Meoru (Vitis coigneties), and analyzed the data with PCA and orthogonal partial least squares discriminant analysis (OPLS-DA). The results showed that there were no significant differences in the primary products from different O. oeni strains, but some important volatile flavor substances (2-phenylethyl alcohol, isoamyl alcohol, 2-butanol, ethyl caprylate, etc.) in its secondary metabolites had significant differences, and these flavor substances were closely related to wine quality［20］. In recent years, many researchers have used metabolome methods to study the effect of the interaction between yeast and lactic acid bacteria on the wine fermentation process. The results of Son et al.［21］ showed that after adding lactic acid bacteria to the Saccharomyces bayanus separate fermentation system, MLF caused decreases in the contents of malic acid and citric acid, and simultaneously increased the content of lactose; and the increase in the content of succinic acid indicated that S. bayanus inhibited MLF. Lopezrituerto et al.［22］ used 9 commercial wine samples as the objects of investigation to investigate the metabolome characteristics of ethanol fermentation and MLF metabolic process, and finally screened out isoamyl alcohol and isobutanol as the biomarkers for distinguishing the authenticity of La Rioja wine by combining MLF with the interval extended canonical variate analysis (iECVA) method. Li et al.［3］ from Northwest A&F University selected 4 kinds of lactic acid bacteria to carry out the lactic acid fermentation of Wada dates and muzao jujube, respectively, and analyzed the physicochemical and flavor quality of fermented jujube juice. It was concluded that the jujube juice could better improve the activity, quality and flavor of lactic acid bacteria after being fermented by lactic acid bacteria. Peng et al.［4］ from Northwest A&F University used 3 strains of compound lactic acid bacteria to study the fermentation of different varieties of apple juice, and studied the flavor and sensory characteristics of different apple juice after fermentation by lactic acid bacteria, and reasonable opinions were given on the suitability of processing apple varieties. Guangpeng LIU et al. Application of Metabonomics in the Research of Lactic Acid Bacteria-fermented Foods
Conclusions
Metabolomics has been widely used in the field of lactic acid bacteria-fermented foods. Due to the complexity of lactic acid bacteria fermentation metabolites and the complexity of the fermented food systems involved, the current quality research and production technical specifications of lactic acid bacteria-fermented foods need to be further improved and perfected. In order to deeply understand the ecological processes and functions of lactic acid bacteria in the food fermentation systems, and reveal the quality improvement mechanism of lactic acid bacteria-fermented foods, future studies of metabolomics in lactic acid bacteria-fermented foods should focus on the following aspects: ① Quenching causes the leakage of lactic acid bacterias intracellular metabolites, which will affect the accuracy of the data results. As a scientific researcher, we should optimize the each lactic acid bacteria quenching method, and establish a perfect and feasible quenching method. ② There is a lack of standardized and comprehensive metabolomics databases. Escherichia coli and Saccharomyces cerevisiae have established relatively complete metabolomics databases, and the metabolic databases of lactic acid bacteria need to be further improved. In order to systematically study biological sciences, a systematic and complete standardized database should be established, so as to improve the connection with other omics and to better interpret the relevant information of organisms, foods, etc. ③ In-depth study can be conducted on the metabolic mechanism of functional lactic acid bacteria from biomarkers to specific metabolic pathways. ④ Genomics, transcriptomics and proteomics can be combined to better interpret the impact of lactic acid bacteria on food quality and human probiotics.
References
［1］ TIAN H, XU X, CHEN C, et al. Flavoromics approach to identifying the key aroma compounds in traditional Chinese milk fan［J］. Journal of Dairy Science, 2019, 102(11): 9639-9650.
［2］ AN F, et al. Metatranscriptome-based investigation of flavor-producing core microbiota in different fermentation stages of dajiang, a traditional fermented soybean paste of Northeast China［J］. Food Chemistry, 2020(343): 128509.
［3］ LI T, JIANG T, LIU N, et al. Biotransformation of phenolic profiles and improvement of antioxidant capacities in jujube juice by select lactic acid bacteria［J］. Food Chemistry, 2020: 127859. ［4］ PENG W, MENG D, YUE T, et al. Effect of the apple cultivar on cloudy apple juice fermented by a mixture of Lactobacillus acidophilus, Lactobacillus plantarum, and Lactobacillus fermentum［J］. Food Chemistry, 2020(340): 127922.
［5］ LIANG H, HE Z, WANG X, et al. Effects of salt concentration on microbial diversity and volatile compounds during suancai fermentation［J］. Food Microbiology, 2020(91): 103537.
［6］ MAZZEI P, PICCOLO A. 1H HRMAS-NMR metabolomic to assess quality and traceability of mozzarella cheese from Campania buffalo milk［J］. Food Chemistry, 2012, 132(3): 1620-1627.
［7］ PIRAS C, MARINCOLA FC, SAVORANI F, et al. A NMR metabolomics study of the ripening process of the Fiore Sardo cheese produced with autochthonous adjunct cultures［J］. Food Chemistry, 2013, 141(3): 2137-2147.
［8］ OCHI H, NAITO H, IWATSUKI K, et al. Metabolomics-based component profiling of hard and semi-hard natural cheeses with gas chromatography/time-of-flight-mass spectrometry, and its application to sensory predictive modeling［J］. Journal of Bioscience & Bioengineering, 2012, 113(6): 751-758.
［9］ RODRIGUES D, SANTOS CH, ROCHA-SANTOS TAP. Metabolic profiling of potential probiotic or synbiotic cheeses by nuclear magnetic resonance (NMR) spectroscopy. Journal of Agricultural and Food Chemistry, 2011, 59(9): 4955-4961.
［10］ SETTACHAIMONGKON S, NOUT MJR, FERNANDES ECA, et al. Influence of different proteolytic strains of Streptococcus thermophilus in co-culture with Lactobacillus delbrueckii subsp. bulgaricus on the metabolite profile of set-yoghurt［J］. International Journal of Food Microbiology, 2014(177): 29-36.
［11］ PALOMO M, et al. Se metallomics during lactic fermentation of Se-enriched yogurt［J］. Food Chemistry, 2014(164): 371-379.
［12］ JUNG JY, LEE SH, LEE HJ, et al. Effects of Leuconostoc mesenteroides starter cultures on microbial communities and metabolites during kimchi fermentation［J］. International Journal of Food Microbiology, 2012, 153(3): 378-387.
［13］ JEONG SH, LEE HJ, JUNG JY, et al. Effects of red pepper powder on microbial communities and metabolites during kimchi fermentation［J］. International Journal of Food Microbiology, 2013.
［14］ ZHAO N, ZHANG C, YANG Q, et al. Selection of taste markers related to lactic acid bacteria microflora metabolism for Chinese traditional Paocai: A GC-MS-based metabolomics approach［J］. J Agric Food Chem, 2016: 2415.
［15］ XU X, WU B, ZHAO W, et al. Shifts in autochthonous microbial diversity and volatile metabolites during the fermentation of chili pepper (Capsicum frutescens L.)［J］. Food Chemistry, 2020(335): 127512. ［16］ KIM J, et al. GC-TOF-MS- and CE-TOF-MS-based metabolic profiling of cheonggukjang (fast-fermented bean paste) during fermentation and its correlation with metabolic pathways［J］. Journal of Agricultural & Food Chemistry, 2012. 60(38): 9746-53.
［17］ KANG HJ, YANG HJ, KIM MJ, et al. Metabolomic analysis of meju during fermentation by ultra performance liquid chromatography-quadrupole-time of flight mass spectrometry (UPLC-Q-TOF MS)［J］. Food Chemistry, 2011, 127(3): 1056-1064.
［18］ NAMGUNG HJ, PARK HJ, CHO IH, et al. Metabolite profiling of doenjang, fermented soybean paste, during fermentation［J］. Journal of the Science of Food & Agriculture, 2010, 90(11): 1926-1935.
［19］ LEE SY, LEE S, LEE S, et al. Primary and secondary metabolite profiling of doenjang, a fermented soybean paste during industrial processing［J］. Food Chemistry, 2014(165): 157-166.
［20］ LEE JE, HONG YS, LEE CH. Characterization of fermentative behaviors of lactic acid bacteria in grape wines through 1H NMR- and GC-based metabolic profiling［J］. Journal of Agricultural & Food Chemistry, 2009, 57(11): 4810.
［21］ SON HS, et al. Metabolomic characterization of malolactic fermentation and fermentative behaviors of wine yeasts in grape wine［J］. Journal of Agricultural & Food Chemistry, 2009. 57(11): 4801-4809.
［22］ LPEZ-RITUERTO E, SAVORANI F, AVENOZA A, et al. Investigations of La Rioja terroir for wine production using 1H NMR metabolomics［J］. Journal of Agricultural & Food Chemistry, 2012, 60(13): 3452-3461.
Key words Metabolomics; Lactic acid bacteria; Fermentation; Food
Received: February 14, 2021 Accepted: April 17, 2021
Supported by Yantai Science and Technology Planing Project (2019ZDCX013); High-efficiency Ecological Agriculture Innovation Project of Taishan Industry Leading Talent Engineering (LJNY202001); Key R&D Program of Shandong Province (2019GNC106019).
Guangpeng LIU (1984-), male, P. R. China, researcher, devoted to research about fruit and vegetable fermentation.
*Corresponding author. E-mail: [email protected].
Lactic acid bacteria have been involved in many fermented food production processes as common strains in fermented foods since ancient times, such as dairy products［1］, soy products［2］, drinks［3-4］ and some pickled foods［5］. The metabolic activities of lactic acid bacteria are closely related to the flavor, aroma, texture and nutrition of fermented foods. With the development of metabonomics technology, this technology has been widely used in the research of monitoring the process of lactic acid bacteria-fermented foods and the formation mechanism of characteristic flavor substances.
Lactic acid bacteria will produce a large number of metabolites during fermentation, including organic acids, amino acids, oligosaccharides, small peptides and some aromatic substances, etc., and revealing the relationship between these metabolites and their influencing factors is of great significance for improving the quality of fermented foods based on lactic acid bacteria and optimizing the fermentation process. The comprehensiveness and high resolution of metabolomics can comprehensively evaluate and discover the subtle differences between samples, so it can provide conclusive and quantitative data for lactic acid bacteria-fermented foods, fermentation process optimization and product quality improvement. Application of Metabonomics in Lactic Acid Bacteria-fermented Drinks
In addition to being widely used in fermented milk and fermented vegetables, lactic acid bacteria also play an important role in the fermentation of some fermented beverages and wines. Lee et al.［20］ used Oenococcus oeni in malolactic fermentation (MLF) of Meoru (Vitis coigneties), and analyzed the data with PCA and orthogonal partial least squares discriminant analysis (OPLS-DA). The results showed that there were no significant differences in the primary products from different O. oeni strains, but some important volatile flavor substances (2-phenylethyl alcohol, isoamyl alcohol, 2-butanol, ethyl caprylate, etc.) in its secondary metabolites had significant differences, and these flavor substances were closely related to wine quality［20］. In recent years, many researchers have used metabolome methods to study the effect of the interaction between yeast and lactic acid bacteria on the wine fermentation process. The results of Son et al.［21］ showed that after adding lactic acid bacteria to the Saccharomyces bayanus separate fermentation system, MLF caused decreases in the contents of malic acid and citric acid, and simultaneously increased the content of lactose; and the increase in the content of succinic acid indicated that S. bayanus inhibited MLF. Lopezrituerto et al.［22］ used 9 commercial wine samples as the objects of investigation to investigate the metabolome characteristics of ethanol fermentation and MLF metabolic process, and finally screened out isoamyl alcohol and isobutanol as the biomarkers for distinguishing the authenticity of La Rioja wine by combining MLF with the interval extended canonical variate analysis (iECVA) method. Li et al.［3］ from Northwest A&F University selected 4 kinds of lactic acid bacteria to carry out the lactic acid fermentation of Wada dates and muzao jujube, respectively, and analyzed the physicochemical and flavor quality of fermented jujube juice. It was concluded that the jujube juice could better improve the activity, quality and flavor of lactic acid bacteria after being fermented by lactic acid bacteria. Peng et al.［4］ from Northwest A&F University used 3 strains of compound lactic acid bacteria to study the fermentation of different varieties of apple juice, and studied the flavor and sensory characteristics of different apple juice after fermentation by lactic acid bacteria, and reasonable opinions were given on the suitability of processing apple varieties. Guangpeng LIU et al. Application of Metabonomics in the Research of Lactic Acid Bacteria-fermented Foods
Conclusions
Metabolomics has been widely used in the field of lactic acid bacteria-fermented foods. Due to the complexity of lactic acid bacteria fermentation metabolites and the complexity of the fermented food systems involved, the current quality research and production technical specifications of lactic acid bacteria-fermented foods need to be further improved and perfected. In order to deeply understand the ecological processes and functions of lactic acid bacteria in the food fermentation systems, and reveal the quality improvement mechanism of lactic acid bacteria-fermented foods, future studies of metabolomics in lactic acid bacteria-fermented foods should focus on the following aspects: ① Quenching causes the leakage of lactic acid bacterias intracellular metabolites, which will affect the accuracy of the data results. As a scientific researcher, we should optimize the each lactic acid bacteria quenching method, and establish a perfect and feasible quenching method. ② There is a lack of standardized and comprehensive metabolomics databases. Escherichia coli and Saccharomyces cerevisiae have established relatively complete metabolomics databases, and the metabolic databases of lactic acid bacteria need to be further improved. In order to systematically study biological sciences, a systematic and complete standardized database should be established, so as to improve the connection with other omics and to better interpret the relevant information of organisms, foods, etc. ③ In-depth study can be conducted on the metabolic mechanism of functional lactic acid bacteria from biomarkers to specific metabolic pathways. ④ Genomics, transcriptomics and proteomics can be combined to better interpret the impact of lactic acid bacteria on food quality and human probiotics.
References
［1］ TIAN H, XU X, CHEN C, et al. Flavoromics approach to identifying the key aroma compounds in traditional Chinese milk fan［J］. Journal of Dairy Science, 2019, 102(11): 9639-9650.
［2］ AN F, et al. Metatranscriptome-based investigation of flavor-producing core microbiota in different fermentation stages of dajiang, a traditional fermented soybean paste of Northeast China［J］. Food Chemistry, 2020(343): 128509.
［3］ LI T, JIANG T, LIU N, et al. Biotransformation of phenolic profiles and improvement of antioxidant capacities in jujube juice by select lactic acid bacteria［J］. Food Chemistry, 2020: 127859. ［4］ PENG W, MENG D, YUE T, et al. Effect of the apple cultivar on cloudy apple juice fermented by a mixture of Lactobacillus acidophilus, Lactobacillus plantarum, and Lactobacillus fermentum［J］. Food Chemistry, 2020(340): 127922.
［5］ LIANG H, HE Z, WANG X, et al. Effects of salt concentration on microbial diversity and volatile compounds during suancai fermentation［J］. Food Microbiology, 2020(91): 103537.
［6］ MAZZEI P, PICCOLO A. 1H HRMAS-NMR metabolomic to assess quality and traceability of mozzarella cheese from Campania buffalo milk［J］. Food Chemistry, 2012, 132(3): 1620-1627.
［7］ PIRAS C, MARINCOLA FC, SAVORANI F, et al. A NMR metabolomics study of the ripening process of the Fiore Sardo cheese produced with autochthonous adjunct cultures［J］. Food Chemistry, 2013, 141(3): 2137-2147.
［8］ OCHI H, NAITO H, IWATSUKI K, et al. Metabolomics-based component profiling of hard and semi-hard natural cheeses with gas chromatography/time-of-flight-mass spectrometry, and its application to sensory predictive modeling［J］. Journal of Bioscience & Bioengineering, 2012, 113(6): 751-758.
［9］ RODRIGUES D, SANTOS CH, ROCHA-SANTOS TAP. Metabolic profiling of potential probiotic or synbiotic cheeses by nuclear magnetic resonance (NMR) spectroscopy. Journal of Agricultural and Food Chemistry, 2011, 59(9): 4955-4961.
［10］ SETTACHAIMONGKON S, NOUT MJR, FERNANDES ECA, et al. Influence of different proteolytic strains of Streptococcus thermophilus in co-culture with Lactobacillus delbrueckii subsp. bulgaricus on the metabolite profile of set-yoghurt［J］. International Journal of Food Microbiology, 2014(177): 29-36.
［11］ PALOMO M, et al. Se metallomics during lactic fermentation of Se-enriched yogurt［J］. Food Chemistry, 2014(164): 371-379.
［12］ JUNG JY, LEE SH, LEE HJ, et al. Effects of Leuconostoc mesenteroides starter cultures on microbial communities and metabolites during kimchi fermentation［J］. International Journal of Food Microbiology, 2012, 153(3): 378-387.
［13］ JEONG SH, LEE HJ, JUNG JY, et al. Effects of red pepper powder on microbial communities and metabolites during kimchi fermentation［J］. International Journal of Food Microbiology, 2013.
［14］ ZHAO N, ZHANG C, YANG Q, et al. Selection of taste markers related to lactic acid bacteria microflora metabolism for Chinese traditional Paocai: A GC-MS-based metabolomics approach［J］. J Agric Food Chem, 2016: 2415.
［15］ XU X, WU B, ZHAO W, et al. Shifts in autochthonous microbial diversity and volatile metabolites during the fermentation of chili pepper (Capsicum frutescens L.)［J］. Food Chemistry, 2020(335): 127512. ［16］ KIM J, et al. GC-TOF-MS- and CE-TOF-MS-based metabolic profiling of cheonggukjang (fast-fermented bean paste) during fermentation and its correlation with metabolic pathways［J］. Journal of Agricultural & Food Chemistry, 2012. 60(38): 9746-53.
［17］ KANG HJ, YANG HJ, KIM MJ, et al. Metabolomic analysis of meju during fermentation by ultra performance liquid chromatography-quadrupole-time of flight mass spectrometry (UPLC-Q-TOF MS)［J］. Food Chemistry, 2011, 127(3): 1056-1064.
［18］ NAMGUNG HJ, PARK HJ, CHO IH, et al. Metabolite profiling of doenjang, fermented soybean paste, during fermentation［J］. Journal of the Science of Food & Agriculture, 2010, 90(11): 1926-1935.
［19］ LEE SY, LEE S, LEE S, et al. Primary and secondary metabolite profiling of doenjang, a fermented soybean paste during industrial processing［J］. Food Chemistry, 2014(165): 157-166.
［20］ LEE JE, HONG YS, LEE CH. Characterization of fermentative behaviors of lactic acid bacteria in grape wines through 1H NMR- and GC-based metabolic profiling［J］. Journal of Agricultural & Food Chemistry, 2009, 57(11): 4810.
［21］ SON HS, et al. Metabolomic characterization of malolactic fermentation and fermentative behaviors of wine yeasts in grape wine［J］. Journal of Agricultural & Food Chemistry, 2009. 57(11): 4801-4809.
［22］ LPEZ-RITUERTO E, SAVORANI F, AVENOZA A, et al. Investigations of La Rioja terroir for wine production using 1H NMR metabolomics［J］. Journal of Agricultural & Food Chemistry, 2012, 60(13): 3452-3461.